Marine multicellular organisms inhabiting waters with natural high fluctuations in pH appear more tolerant to acidification than conspecifics occurring in nearby stable waters, suggesting that environments of fluctuating pH hold genetic reservoirs for adaptation of key groups to ocean acidification (OA). The abundant and cosmopolitan calcifying phytoplankton Emiliania huxleyi exhibits a range of morphotypes with varying degrees of coccolith mineralization. We show that E. huxleyi populations in the naturally acidified upwelling waters of the Eastern South Pacific, where pH drops below 7.8 as is predicted for the global surface ocean by the year 2100, are dominated by exceptionally overcalcified morphotypes whose distal coccolith shield can be almost solid calcite. Shifts in morphotype composition of E. huxleyi populations correlate with changes in carbonate system parameters. We tested if these correlations indicate that the hypercalcified morphotype is adapted to OA. In experimental exposures to present-day vs. future pCO2 (400 µatm vs. 1200 µatm), the overcalcified morphotypes showed the same growth inhibition (−29.1 ± 6.3 %) as moderately calcified morphotypes isolated from non-acidified water (−30.7 ± 8.8 %). Under OA conditions, production rates of particulate organic carbon (POC) increased, while production rates of particulate inorganic carbon (PIC) were maintained or decreased slightly (but not significantly), leading to lowered PIC/POC ratios in all strains. There were no consistent correlations of response intensity with strain origin. OA affected coccolith morphology equally or more strongly in overcalcified strains compared to moderately calcified strains. OA conditions appear not to directly select for exceptionally overcalcified morphotypes over other morphotypes directly, but perhaps indirectly by ecologically correlated factors. More generally, these results suggest that oceanic planktonic microorganisms, despite their rapid turn-over and large population sizes, do not necessarily exhibit adaptations to naturally high CO2 upwellings, and this ubiquitous coccolithophore may be near a limit of its capacity to adapt to ongoing ocean acidification.